Novel molecular determinants of viral susceptibility and resistance in the lipidome of Emiliania huxleyi

Abstract

Viruses play a key role in controlling the population dynamics of algae, including Emiliania huxleyi, a globally distributed haptophyte with calcite coccoliths that comprise ca. 50% of the sinking carbonate flux from the surface ocean. Emiliania huxleyi viruses (EhVs) routinely infect and terminate E. huxleyi blooms. EhVs are surrounded by a lipid envelope, which we found to be comprised largely of glycosphingolipids (GSLs) with lesser amounts of polar glycerolipids. Infection appears to involve membrane fusion between the virus and host, and we hypothesized that specific polar lipids may facilitate virus attachment. We identified three novel intact polar lipids in E. huxleyi strain CCMP 374 and EhV86, including a GSL with a monosaccharide sialic acid headgroup (sGSL); for all 11 E. huxleyi strains we tested, there was a direct relationship between sGSL content and sensitivity to infection by EhV1, EhV86 and EhV163. In mesocosms, the E. huxleyi population with greatest initial sGSL content had the highest rate of virus-induced mortality. We propose potential physiological roles for sGSL that would be beneficial for growth but leave cells susceptible to infection, thus furthering the discussion of Red Queen-based co-evolution and the cost(s) of sensitivity and resistance in the dynamic E. huxleyi-EhV system.

Rewiring Host Lipid Metabolism by Large Viruses Determines the Fate of Emiliania huxleyi, a Bloom-Forming Alga in the Ocean

“…In vitro studies showed that the EhV-encoded SPT preferentially utilizes myristoyl-CoA as a substrate, rather than the classical host SPT that uses palmitoyl-CoA (Han et al, 2006). Indeed, production of viral-derived sphingolipids (e.g., vGSL) was recently demonstrated and suggested to have a functional role in viral assembly as they are major constituents of viral membranes (Vardi et al, 2009(Vardi et al, , 2012Fulton et al, 2014). Our metabolome analysis clearly indicated increased levels of fatty acids, amino acids, and glucose.…”

“…Specific fingerprinting of viral-derived sphingolipids revealed a unique signature of multihydroxylated C16-based long-chain base forms in infected cultures and natural populations (Vardi et al, 2012;Fulton et al, 2014).…”

“…Areas of metabolites were normalized to the area of the IS and to the amount of algae used for analysis. Detection of vGSL, hGSL, and sGSL was made according to Vardi et al (2009), Vardi et al (2012, and Fulton et al (2014).…”

“…Glycosphingolipids, a subgroup of sphingolipids, are common constituents of membrane lipids and lipid rafts in eukaryotes. EhV is enveloped by lipid membranes (Mackinder et al, 2009), which are composed mainly of viral glycosphingolipids (vGSLs) (Fulton et al, 2014). These bioactive lipids can induce host programmed cell death (PCD) in lytic infected cells (Vardi et al, 2009(Vardi et al, , 2012.…”

Targeted and untargeted lipidomics of Emiliania huxleyi viral infection and life cycle phases highlights molecular biomarkers of infection, susceptibility, and ploidy

“…Under lytic infection however, viral glycosphingolipids (vGSLs) derived from myristoyl-CoA are synthesized de novo, and vGSLs are known to play a role in the regulation of cell death in infected cells and are enriched in the membrane of newly formed virions (Vardi et al, 2009;Fulton et al, 2014;Rosenwasser et al, 2014). These vGSLs were detected in coccolithophore populations in the North Atlantic, which highlights their potential as biomarkers for viral infection in the oceans (Vardi et al, 2009(Vardi et al, , 2012.…”